Amencan Museum
ovitates
PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 7QTH STREET, NEW YORK, N. Y. 10024
NUMBER 22094 JUNE 28, 1967
Speciation in Colombian Forest Birds West
of the Andes
By Jiincen Harrer!
INTRODUCTION
The Cordilleras of the northern Andes separate a narrow, humid,
tropical lowland forest belt, along the Colombian Pacific coast, from
the extensive Amazonian basin east of the mountains. The humid forest
extends into Central America. This trans-Andean forest region? is char-
acterized by a surprisingly large number of endemic birds. Chapman
(1917, p. 106) called the fauna of the Pacific lowlands of Colombia “the
most circumscribed and sharply defined, and possibly the most strongly
characterized of any fauna of South America.”
It is the thesis of the present paper that the faunas west of the Andes
were more influenced by climatic changes during the Pleistocene and
post-Pleistocene than by orogenic events. The isolation and differentia-
tion of most trans-Andean species occurred after the early Pleistocene
uplift of the northern Andes and probably under orographic conditions
essentially the same as those that exist at the present time.
This paper is divided into two major parts. The distribution of tropi-
cal lowland forests in northwestern South America, the probable geo-
1 Geologist, Colombian Petroleum Company, Apartado Aereo 3434, Bogota, Colombia.
2 The tropical lowlands west of the Andes in Colombia and in Central America are
designated in this paper as “trans-Andean” or “Pacific,” and those east of the Andes
as “cis-Andean” or “Amazonian.” Geographically and historically (with respect to the
evolution of the lowland bird faunas) this usage seems preferable to that of Chapman
(1917, 1926) who sometimes referred to “cis-Andean” and “trans-Andean” in the op-
posite sense.
2 AMERICAN MUSEUM NOVITATES NO. 2294
logical and climatic history, and the historic interpretation of the speci-
ation of trans-Andean forest birds are given in the first part. In the
second part I describe the results of my ornithological field work, espe-
cially with respect to the occurrence of narrow zones of allopatric
hybridization in the Uraba region of northwestern Colombia. Multiple
invasions into the trans-Andean region and an analysis of the Chocd
fauna of western Colombia are also briefly discussed.
I spent a total of 23 months in the north Colombian lowlands when
conducting geological field work in the area around the Gulf of Uraba,
in the Atrato Valley, in Bolivar, and on the Guajira Peninsula during
the years 1958 to 1966. A skin collection of approximately 1000 speci-
mens made in these areas was divided between the Instituto de Ciencias
Naturales, Universidad Nacional, in Bogota, and the American Museum
of Natural History, and has been discussed elsewhere (Haffer, 1959,
1961, 1962, and in press, a; Haffer and Borrero, 1965).
My thanks are due to Father A. Olivares, head of the Ornithology
Department of the Instituto de Ciencias Naturales in Bogota, who per-
mitted me to use freely the collections and the library of the Instituto.
I gratefully acknowledge critical comments and numerous helpful sug-
gestions from Prof. Erwin Stresemann who kindly read the typescript.
Mr. Eugene Eisenmann has patiently answered many questions concern-
ing the distribution of Central American birds and discussed several
aspects of this article with me. I wish to express my sincere thanks to
him for his generous help and important suggestions. Dr. Ernst Mayr
has read an early stage of the manuscript and also offered critical re-
marks. Dr. E. O. Willis kindly permitted me to include his unpublished
observations on hybridization of manakins in northern Colombia. The
following persons have furnished me with valuable information: Dr.
Alexander Wetmore, Mr. Rodolphe M. de Schauensee, Mr. J. D. Mac-
donald, Dr. Maria Koepcke, Dr. H. Sick, Dr. Charles G. Sibley, and
Mr. F. Vuilleumier. I must also thank my father, Dr. O. Haffer, who
gave much of his time to prepare and send to Colombia copies and
summaries of published articles not available to me. I am most grateful
to Dr. Dean Amadon and Mr. Eisenmann for their painstaking help in
the preparation of the manuscript for publication.
PRESENT DISTRIBUTION OF TROPICAL LOWLAND FORESTS
IN NORTHWESTERN SOUTH AMERICA
The lowlands to the north, east, and west of the Colombian Andes
are in part covered with extensive forests (fig. 1), although recent burn-
ing and clearing have reduced the drier woodlands to an alarming extent
1967 HAFFER: COLOMBIAN BIRDS 3
Fic. 1. Present distribution of tropical lowland forest in northwestern South
America and southern Central America. The forests of the upper Orinoco region
are influenced by the trade-wind climate and show characters of the Dry Tropi-
cal Forest (Hueck, 1966, p. 56). Elevations over 1000 meters are in black.
Adapted from Chapman (1926), Hueck (1960), Koepcke (1961), Lauer (1959),
Slud (1964), Eisenmann (im /itt.), Espinal and Montenegro (1963), and author’s
observations in Colombia.
Key: 1. Dry open areas and natural savannas, i.e., llanos. 2. Artificial savan-
nas and secondary growth with some remnants of Dry Forest (or of Moist
Forest, chiefly in Caribbean Costa Rica and Panama). 3. Dry Forest: 1000
to 2000 mm. of rain per year. 4. Moist Forest: 2000 to 4000 mm. of rain per
year. 5. Wet Forest: 4000 to 8000 mm. of rain per year. 6. Pluvial Forest:
More than 8000 mm. of rain per year.
in more accessible areas. The immense Amazonian forests of southeastern
Colombia are still relatively untouched except at the foot of the Andes
where large clearings exist around major villages and towns. Toward the
4 AMERICAN MUSEUM NOVITATES NO. 2294
grass plains of the llanos these forests are interspersed with natural
savannas of varying sizes. The forests continue northward along the foot
of the Eastern Cordillera as a narrow band and cover the southern slope
and foot of the Venezuelan Mérida Andes. The Maracaibo forests of
the Catatumbo lowlands are directly connected with the forests on the
western slope of the Serrania de Perija. This forest connection is evi-
dent in the Montes de Oca at the northern end of the Serrania de Perija.
The open woods that originally covered the north Colombian plains
have largely disappeared; only small remnants are still preserved in the
valleys of low ranges close to the Caribbean coast (Serrania de San
Jacinto). More extensive forests are found at the northern end of the
Central and Western Cordilleras of Colombia and in the humid middle
Magdalena Valley. These forests are broadly connected around the Gulf
of Uraba with the wet and heavily forested region west of the Andes
along the Pacific coast of Colombia and northwestern Ecuador. The
trans-Andean humid forests continue northwestward into Middle Amer-
ica, covering most of the Caribbean slope from Panama to Mexico and
smaller portions of the Pacific slope, particularly in the Darién region
of eastern Panama and in southwestern Costa Rica.
It should be noted that large tracts of the more accessible forests have
disappeared on account of the activity of man during the last centuries
and are being destroyed daily. The more humid sections have suffered
less from burning and clearing, and parts are currently being set aside
as forest reserves in the hope of ensuring their preservation.
The above brief outline of the forest distribution in northwestern South
America indicates a connection of the trans-Andean forests with the
Amazonian basin, through narrow humid areas along the Caribbean
slope at the northern foot of the mountain ranges in northern Colombia
and northwestern Venezuela.
For a modern comprehensive treatment of the neotropical forests, see
a recent work by K. Hueck (1966) which gathers the widely scattered
literature and describes the ecology and distribution of the various plant
formations of South America.
GEOLOGIC AND CLIMATIC HISTORY
TERTIARY
The Colombian cordilleras developed during Tertiary time when they
were composed of low-lying, hilly, and in part swampy, country. The
fauna of these Tertiary “Andes” of Colombia was probably poor, since
the mountain chains were separated from one another and from the
large land areas north and south of the present Amazon River by ex-
1967 HAFFER: COLOMBIAN BIRDS 5
tensive shallow seas, lakes, and marshes, until the end of the Pliocene
(fig. 2). During the Tertiary (Upper Eocene) an archipelago was formed
in the region of present Central America, which allowed temporary
exchange of some terrestrial forms (Simpson, 1950; Belding, 1955;
Birgl, 1961). The basalt ranges of the Colombian coastal cordillera,
including the mountains of southeastern Darién in Panama (Mt. Sapo,
Mt. Pirri), probably formed part of this rather old archipelago (for a
TERTIARY 5 | °
2.U. MIOCENE
TERTIARY 6
PLIOCENE
|. M. MIOCENE
UZ MARINE FACIES
[? — 4 ‘
(J MARINE ay +2 \ nf Pts
5 ~ [J conrimentar Facies
[7] continenra aye et
Ae, EA
ea : i
(7774 wixeo Facies
wxeo
VOLCANICS
VOLCANICS
Fic. 2. Paleogeographic maps of South America during upper Tertiary time.
Left: Middle and Upper Miocene. Right: Pliocene. After Harrington (1962).
discussion of the Central American ocean channels connecting the Pacific
and Caribbean, see Darlington, 1957; Slud, 1960; Lloyd, 1963; Mayr,
1964).
The last gap separating Central and South America was probably not
in Panama but just south of the Gulf of Uraba in Colombia. This sea-
way connected the Caribbean Sea and the Pacific Chocé basin of west-
ern Colombia (Haffer, MS; Woodring and Thompson, 1949; Simpson,
1950). It was not closed until late Pliocene time.
PLEISTOCENE
The rather low mountain ranges of the Tertiary Colombian Andes
were probably uplifted to about their present height at the beginning
6 AMERICAN MUSEUM NOVITATES NO. 2294
of the Pleistocene. At the same time the surrounding lowlands of western
and northern Colombia emerged, became forest covered, and thus habit-
able for the forest fauna of the Amazonian region. Extensive vestiges
of the Pleistocene glaciations have been found in the Colombian Andes
which are ascribed to the younger Riss and Wiirm glacials (Wilhelmy,
1957; van der Hammen and Gonzalez, 1960; Birgl, 1961). The fact that
no moraines of the older Giinz and Mindel glaciations are known so
far in Colombia has led some authors to assume that the northern Andes
had not attained sufficient elevation at that time. However, more con-
clusive evidence is needed to substantiate this assumption.
A similar glaciation was recently discovered by Weyl (1956) in the
highest peaks of the Cordillera de Talamanca of Costa Rica.
The glaciation of the South and Central American mountain ranges
indicates a Pleistocene refrigeration in the tropics. The temperature re-
duction from that prevailing at present is believed to have amounted to
approximately 3° to 4° C. in the lowlands (Mayr and Phelps, 1955;
Wilhelmy, 1957), but reached 7° to 8° C. in the higher elevations of
the mountains (van der Hammen and Gonzalez, 1960; van der Hammen,
1961). Under such circumstances the temperature gradient in at least
parts of the tropics must have been greater during the cold glacial periods
than it is today, possibly 0.8°-0.9° C. per 100 meters compared to the
present 0.5°-0.6° C. per 100 meters (Mortensen, 1957), and the climatic
transition from the tropical lowlands to the cool mountain zones would
have been more abrupt. Also the transition zone from the tropics in
South and Central America to the temperate zone in the southern United
States was probably much narrower during the glacials than it is today,
which means that the southward shift of the boundaries between glaci-
ated to non-glaciated areas (arctic to temperate zone, temperate zone to
subtropical zone, and subtropical to tropical zone) decreased progressively
southward (toward the equator). In other words the tropical zone as such
was only slightly reduced latitudinally and altitudinally by the southward-
moving glaciers (and in the mountains from the downward moving gla-
ciers). Certainly the reduction of the tropics was much less than one would
assume from the southward push of the glaciated arctic zone alone. The
faunas of the cool “temperate” and “subtropical” life zones on tropi-
cal mountains were able to extend their distributions considerably during
the glacial periods, occupying relatively low ridges of only 1000 to 1200
meters and 400 to 600 meters in elevation, respectively, the latter being
today completely within the hot tropical climate. Moreover, such low
isolated ranges had a slightly higher elevation than they have today,
owing to the Pleistocene lowering of the sea level, and these ranges
1967 HAFFER: COLOMBIAN BIRDS 7
formed important stepping stones for at least part of the fauna of the
cooler mountain zones across the lowlands (which remained in the tropi-
cal zone even at the height of the Pleistocene refrigeration).
A probable increase of the temperature gradient in Africa during the
glacial periods of the Pleistocene is indicated by the data summarized
by Mortensen (1957) and Moreau (1963). The reduction of the average
temperature in this region was calculated by various authors at about
4° C. at sea level, and a drop of 6°, 7°, and 8° C. probably occurred
Fic. 3. Northern Colombia during the glacial and interglacial periods of the
Pleistocene. The present coast line is dotted; elevations over 1000 meters are
in black. Left: Glacials: Climate humid and sea level lowered by about 100
meters. Arrows indicate advancing cis-Andean and trans-Andean forest faunas.
Right: Interglacials: Climate dry in northern half and sea level raised by 30
to 50 meters. I. Chocé Refuge; II. Nechi Refuge.
on Mt. Ruwenzori, Mt. Kilimanjaro, and in the highlands of Ethiopia,
respectively.
The northern tip of South America (Guajira Peninsula) was in the
tropical zone during the glacial periods (Wilhelmy, 1954), as were the
lowlands of Colombia and great parts of Central America. That the
tropical zone reached as far north as Mexico during the height of glacia-
tion appears to be possible (Martin, 1958) but remains questionable.
The Pleistocene temperature changes were of much less importance to
the fauna of the South American tropical lowlands than the periodic
changes from dry to humid climates. The glacial periods were much
more humid in tropical America than the interglacials. Wilhelmy (1954)
has pointed out that there was an increase of precipitation in the tropics
of South America during the glacials due to an extension of the equa-
8 AMERICAN MUSEUM NOVITATES NO. 2294
torial rain belt and a corresponding compression of the dry trade-wind
belt of the Northern Hemisphere. For this reason the north Colombian
lowlands, including the now arid Guajira Peninsula, were forest-covered
much more extensively during the humid glacial periods than they are
today, thus providing a broad connection of the Amazonian faunal re-
gion with the trans-Andean faunal area of western Colombia and Central
America. This effect was increased by the lowering of the sea level by
approximately 100 meters. On the other hand, during the drier inter-
glacials, the north Colombian connection of the cis- and trans-Andean
forests was interrupted when the humid vegetation retreated southward,
owing to a strengthened influence of the trade winds in this area, and
the sea level rose by about 30 to 50 meters, thus flooding great parts
of the Maracaibo basin and large portions of the north Colombian
plains (fig. 3).
Post-PLEISTOCENE
The shifting of humid and dry zones and alternation of humid and
dry periods in South and Central America continued during post-Pleisto-
cene time (van der Hammen and Gonzalez, 1960; van der Hammen,
1961). Evidence for a more humid climate in the recent past in regions
that at present are arid has been collected by Wilhelmy (1954). He
found fossil valleys and peat deposits on the islands of Aruba and Bon-
naire, thick gravel beds in the Cesar Valley of northeastern Colombia,
calcareous tufas, crusts, and limonite concretions on the Guajira Penin-
sula, and fossil red soils on Curacao and near Maracaibo. These deposits
could not have been formed in these areas under the present arid climate.
On the other hand, Goosen (1964) described long, narrow sand dunes
from the humid llanos of eastern Colombia. They run in a northeasterly
direction of the trade winds and were formed during a sub-Recent period
of drought. The widely scattered small patches of “campos cerrados”
within the Amazonian forest region are also considered evidence for a
previously much wider distribution of this plant formation when the
forests were more restricted because of different climatic conditions
(Hueck, 1966).
At present only the fact of repeated climatic changes and a corre-
sponding shifting of the vegetation zones during the Pleistocene and
post-Pleistocene can be demonstrated for the Neotropical Region. It is
left for future investigators to study the distribution of forest and non-
forest vegetation in different areas during each of the various climatic
periods as is being done in Africa, where a great amount of detail has
already been accumulated (Moreau, 1963).
1967 HAFFER: COLOMBIAN BIRDS 9
TRANS-ANDEAN FOREST REFUGES AS CENTERS
OF BIRD SPECIATION
Forest REFUGES
The cis- and trans-Andean forests have been broadly connected in the
north Colombian lowlands during the humid climatic periods of the
Pleistocene and post-Pleistocene. An exchange of the eastern and western
faunas around the northern tip of the Andes was further facilitated by
the Pleistocene lowering of the sea level which resulted in a considerable
expansion of the Caribbean lowlands north of the Andes. Amazonian
forms that had come around the Andes in the north followed the Colom-
bian Pacific coast southward, or occupied parts of Central America, or
advanced in both directions (fig. 3).
During the interglacials and the post-Pleistocene dry climatic periods
the humid forests were pushed southward on each side of the Andes and
were replaced by drier types of vegetation. The Central American forests
probably were also considerably reduced, with only parts of the north-
eastern slope of the higher cordilleras left forest-covered. These forests
received rains from the winds that, in blowing against the mountains,
were sharply cooled by the abrupt slope. I believe, on the basis of the
present rainfall pattern in the Uraba area (Schmidt, 1952; and West,
1957), that the connection of the Central American and the west-
Colombian forests was interrupted in the Uraba-lower Atrato region
during these dry periods when the effect of the trade winds was here
more pronounced than at present. Even the lowlands of central and
eastern Panama were probably devoid of heavy forests in most areas
(see also Haffer, in press, a).
Recently Reichel-Dolmatoff (1965, pp. 42-44) made a similar sug-
gestion when discussing the immigration of prehistoric man into north-
ern Colombia. He said “that climatic changes during Late Pleistocene
times would have influenced the Darien landscape and that during drier
periods the jungle growth would have largely disappeared and a route
[for human migrations] would have presented itself,” and “a southward
shift of 2° of the present border of savannah climate in northern Colom-
bia would clear the route to South America.”
A number of forest refuges presumably existed during these dry periods
which were effectively isolated from one another and from the great
“Amazonian Refuge” east of the Andes. They may be named and briefly
described as follows (fig. 4):
CENTRAL AMERICAN REFUGES -
CarIBBEAN Reruces: Several rather extensive refuges probably existed along
the Caribbean slope of the Central American mountains in Guatemala, Hon-
10 AMERICAN MUSEUM NOVITATES NO. 2294
T.CARIBBEAN COSTA RICA-Refuge
=
AS =Anyy
as
Pteroglossus , Cyanerpes
7
Galbula , ieuaseo re
Aramides, Formicarius
Fic. 4. Trans-Andean forest refuges during Pleistocene and post-Pleistocene
periods of drought. Zones of secondary contact, possible overlap, or hybridiza-
tion in Caribbean western Panama and in the Uraba region are indicated by
dashed lines (for species involved, see table 2). Other forest refuges existed along
the Caribbean slope of Central America north of the area shown.
duras, Nicaragua, and Costa Rica. Many of the endemic bird forms of the
Caribbean forests originated in these refuges. The southernmost refuge may
be called the “Caribbean Costa Rica Refuge.” It comprised the foothills and
adjacent lowlands of the Guanacaste, Central, and Talamanca mountains of
Costa Rica. Endemic forms of this refuge are: Trogon clathratus, Tangara f. florida,
Bangsia arcaet, and Heterospingus (xanthopygius) rubrifrons.
Cuirigui Reruce: This comprised the Pacific slope of southwestern Costa
Rica and extreme western Panama. The following forms differentiated in this
area are so well marked that they must be considered semispecies, if not good
species: Trogon (viridis) bairdit, Pteroglossus (torquatus) frantzit, Thamnophilus bridges,
Thryothorus (nigricapillus) semibadius, and others.
CoLoMBIAN REFUGES
Cuocé Reruce!: This comprised the central portion of the Pacific lowlands
of Colombia. The bulk of the west-Colombian birds originated in this refuge
area; a few are still restricted to its previous extent: Columba (Oenoenas) goodsoni,
1“Chocé” is the name of an Indian tribe inhabiting the lowlands of the Atrato and
San Juan rivers (West, 1957). The Departamento Chocé comprises the northern half of
the Pacific lowlands of Colombia.
1967 HAFFER: COLOMBIAN BIRDS 11
Pittasoma rufopileatum, Tangara johannae, Tangara florida auriceps.
Necui Reruce!: In forests along the northern foothills and adjacent low-
lands of the Central and Western Cordillera of Colombia. The more important
forms that probably originated here are: Crypturellus (boucardi) columbianus, Crax
alberti, Pionopsitta pynitia, Trogon melanurus macroura, Brachygalba salmont, Nonnula
frontalis, Capito hypoleucus, Thamnophilus nigriceps, Dacnis viguiert, Tangara inornata,
Habia gutturalis, and Gymnostinops guatimozinus.
In addition other isolated forests may have existed on the northern or
northeastern (or both) slopes of some of the mountain massifs of eastern
Panama (i.e., Mt. Pirri, Mt. Tacarcuna) and in the Serrania de Perija.
An example of a forest refuge within the present trade-wind desert
zone along the northern coast of South America is on the arid Guajira
Peninsula of northeastern Colombia. The large plains of this peninsula
are covered only with scattered cacti and scrub (Haffer, 1961). The low
mountain range of the Serrania de Macuira (300 to 800 meters in eleva-
tion) close to the tip of the peninsula catches the winds from the Carib-
bean Sea. For this reason its northeastern flank is covered with a moist
forest vegetation which is completely isolated from the woodlands at
the base of the peninsula some 150 kilometers away. A number of bird
species living in this forest belt in most cases are already differentiated
as well-marked subspecies: Ortalis ruficauda lamprophonia,? Momotus momota
spatha, Thryothorus leucotis collinus, Turdus leucomelas cautor, Cyanerpes cyaneus
gemmeus, Hylophilus flavipes melleus, and Arremon schlegelt fratruelis (Wetmore,
1941, 1946, 1953).
During the dry climatic periods of the Pleistocene and post-Pleistocene
the fauna of the more open and arid areas east of the Andes advanced
into northern Colombia and followed the Magdalena Valley, which was
devoid of heavy forest and more or less arid in its entire length; the un-
forested regions around the Gulf of Uraba offered a pathway through
Panama into Central America. At the same time the fauna of the more
arid portions of Middle America invaded northern South America. The
return of more humid conditions interrupted the connection of the
Central American and north Colombian open-country fauna which then
retreated into several small dry refuges, ie., along the Pacific coast of
Central America, in the upper Magdalena Valley, the Patia Valley, and
other intermontane valleys in the rain shadow of the surrounding
mountains.
1 After the Rio Nechi, which flows down the northern slope of the Central Cordillera
and joins the Cauca River at the village of Nechi.
2 This subspecies was not recognized by Vaurie (1965) in his recent revision of Ortaits.
3 A historic interpretation of the differentiation of the non-forest faunas of north-
western South America is given elsewhere (Haffer, in press, b).
12 AMERICAN MUSEUM NOVITATES NO. 2294
SPECIATION
The bird populations of the trans-Andean forest refuges were isolated
from one another and from the great population of the Amazonian
basin. A gene exchange was prevented by the intervening arid areas
and the mountain ranges. It is concluded that the numerous endemic
forms of the Central American and west-Colombian lowland forests
originated as peripheral isolates of the large Amazonian population.
The present situation is the result of several such processes of geo-
graphic isolation during the Pleistocene and post-Pleistocene. It is reason-
able to assume that forms only weakly differentiated were isolated rather
recently, and that strongly marked populations had been cut off west of
the Andes much earlier. However, this situation may be reversed in con-
servative and plastic species, respectively.
ALLOPATRIC HYBRIDIZATION
The process of differentiation of an isolated bird population is gradual
and progresses slower or faster according to various conditions such as
the size of the population. For this reason every conceivable stage be-
tween the “subspecies” and “species” level was reached by trans-Andean
isolates when they again came into contact with other trans-Andean
refuge populations or with the Amazonian population during a later
humid period. Those forms that had not developed sufficient premating
sexual isolating mechanisms (Mayr, 1963) hybridized along zones of
secondary contact. The width of such belts of allopatric hybridization
varies considerably (Mayr, 1942, 1963).
A broad zone of secondary intergradation is found between the Costa
Rican wren Thryothorus nigricapillus costaricensis and T. n. schotti of western
Colombia; it comprises the whole of central and eastern Panama (Wet-
more, 1959). In this species the chestnut-breasted form, costaricensis,
probably originated in the Caribbean Costa Rica Refuge, whereas the
subspecies schottiz, with the anterior under parts barred black and white,
was differentiated in the Chocéd Refuge. Closer examination of those
many forest species that are continuously distributed around the northern
tip of the Andes will probably show in some cases that the trans- and
cis-Andean populations are connected by broad zones of secondary inter-
gradation, with stepped clines developed in northern Colombia or north-
western Venezuela, or both.
Narrow zones of allopatric hybridization are developed along the
eastern margin of the Caribbean Costa Rica Refuge and at the northern
margin of the Chocdéd Refuge (fig. 4). In the first case Amazonian and
1967 HAFFER: COLOMBIAN BIRDS 13
Chocé elements made contact with Central American forms that orig-
inated in one of the Caribbean refuges. In the second case Amazonian
and Central American forms met Chocé elements in the Uraba region.
Hysrip Zones ALONG EasTERN MarcIN OF CaRIBBEAN Costa RICA
Reruce: On the Panama-Costa Rica border Chalybura (urochrysia ) melanorrhoa
intergrades with C. u. isaurae along a rather narrow zone (Eisenmann and
Howell, 1962). Other allopatric “species” that meet or almost meet in
the Caribbean lowlands of extreme western Panama or adjacent Costa
Rica include the following: Manacus vitellinus and M. candei (see below);
Ramphocelus flammigerus icteronotus! and R. passerinit; Phloeceastes melanoleucus
and P. guatemalensis. The partners of the latter two “species” pairs are
known to replace each other abruptly in the lowlands at the Chiriqui
lagoon of western Panama (Peters, 1931).
Hysrip Zones AT NORTHERN Marcin ofr Cuocd Reruce: The partners
of the two semispecies” pairs Pteroglossus torquatus and P. (t.) sanguineus,
also Galbula ruficauda and G. (r.) melanogenia intergrade along narrow
zones in the Uraba area (see detailed discussion in the second part of
this paper). The following well-marked allopatric forms are still treated
as “species” in formal lists, but they apparently meet and may also
hybridize along narrow zones in this region. However, the zone of con-
tact is not yet sufficiently known in these cases for a definite conclusion
to be reached regarding their relationship: Aramides cajanea and A. wolf,
Formicarius analis and F. nigricapillus, Glaucis hirsuta and G. aenea, Cyanerpes
caeruleus and C. lucidus, Gymnostinops guatimozinus and G. cassint.
Aramides cajanea inhabits the lower Atrato region (Rio Salaqui, Jurado),
but A. wolfi is known from the central Chocé to the south. Both forms
are reported from the Alto del Buey area which, however, does not
prove sympatric breeding (for details of distribution in this case and the
following, see de Schauensee, 1948-1952). The distribution of the Formi-
cartus forms is very similar to that of Aramides: F. nigricapillus is found in
the Chocé lowlands north to Nuqui and the Rio Jurubida on the Pacific
coast, and F. analis inhabits the Urabd region and the Atrato Valley.
The nearest localities where these forms have been taken are approxi-
mately 80 kilometers apart. Both birds are inhabitants of the humid low-
1 Sibley (1958) has shown that R. flammigerus (Jardine and Selby, 1833) of the Cauca
Valley of Colombia hybridizes freely with R. icteronotus (Bonaparte, 1838) of the Pacific
lowlands.
2 Semispecies are defined as “populations that have acquired some, but not yet all,
attributes of species rank” (Mayr, 1963, p. 671). As proposed by Lorkovié (1958), the
name of the species of which a semispecies forms part is enclosed in parentheses. A
semispecies may be monotypic or may consist of several clinal forms, which are desig-
nated as a “‘subspecies group” in this paper.
14 AMERICAN MUSEUM NOVITATES NO. 2294
lands in western Colombia and may meet somewhere in the Alto del
Buey area. Glaucis aenea occupies the Chocé lowlands north to Andagoya
and Nuqui, whereas G. hirsuta was collected along the entire Atrato Val-
ley south to Quibddé. The only locality at which both forms seem to
have been taken is Santa Cecilia, Caldas.! The fact that both Cyanerpes
caeruleus chocoanus and C. lucidus isthmicus have been taken along the Rio
Jurad6 is no proof that they are sympatric breeders. However, so far no
intergrades have been collected between any of the above-mentioned
allopatric forms. The Nechi form Gymnostinops guatimozinus meets G. cassini
in the Salaqui area. Two skins from this river are close in coloration to
G. guatimozinus, “but the male shows a tinge of chestnut on the sides of
the body. The head, upper mantle and underparts are glossed with green;
this is not as intense as in guatimozinus. They are in a sense slightly inter-
mediate between guatimozinus from Darién and cassint from the Rio
Baud6é” (R. M. de Schauensee, in /itt., and 1966). These birds may in-
dicate the existence of a narrow hybrid zone between both forms in the
lower Atrato Valley.
HyspripizaTion IN Manacus (Fic. 5): The cis-Andean white-breasted
form M. manacus is represented west of the Andes by the yellow-breasted
M. ovitellinus (which extends through Panama), and in Caribbean Central
America by Manacus candei. These strictly allopatric forms have hitherto
been considered specifically distinct from each other, although no de-
tailed study of their zones of secondary contact has so far been under-
taken. Recent observations by E. O. Willis at Caucasia on the lower Rio
Cauca (fig. 5, 1) indicate that Manacus manacus abditivus and M. ottellinus
millert hybridize freely where their ranges meet in northern Colombia:
“At Caucasia, in an isolated woodlot in the pastures four kilometers
west of town and by the road, I found males of both types displaying
in the same dancing ground, no more than ten meters apart. In between
males of seemingly pure types in this same dancing ground, there were
several intermediate or hybrid males displaying. Out of some ten males
displaying in this small dancing ground, two at the north end were
white, one or two at the south end were yellow and six or so in between
were pale yellow in the parts of the plumage which differ in the two
1 Santa Cecilia is at the foot of the Western Andes on the upper Rio San Juan. These
Glaucis forms probably meet near this locality, because E. Eisenmann (in itt.) has com-
pared one “male?” aenea (and apparently such) and one “female” (obviously immature,
and agreeing with G. hirsuta affinis), both of which were collected near Santa Cecilia at
2400 feet on November 17 and 19, 1945, respectively. These specimens were kindly sent
to Eisenmann by Mr. de Schauensee. The latter’s statement (1966) that these forms
“occur together commonly on the Pacific slope of Colombia” is still unproved.
1967 HAFFER: COLOMBIAN BIRDS 15
candei- Group
vitellinus-Group
0°
Fic. 5. Distribution of Manacus manacus (Linnaeus).
Key: Vertical lines, Manacus manacus; dotted area, Manacus (manacus ) vitellinus;
horizontal lines, Manacus (manacus) candei. Plumage color key: Dashed, gray;
hatched, green; dotted, yellow; unmarked, white; solid, black. See text for
numbered localities.
taxa. I collected one of the pale yellow birds (Museum of Vertebrate
Zoology No. 148-593) and one of the white birds (MVZ No. 148-592),
using mist nets set about four meters apart.
“Examination of the hybrid male from Caucasia and comparison with
specimens of Manacus vitellinus miller here at The American Museum of
Natural History show that it is like mzllerx but much paler on the under-
parts and collar. The collar and cheeks are especially pale, being straw
16 AMERICAN MUSEUM NOVITATES NO. 2294
yellow like the throat and breast rather than bright yellow. The collar
is wider than in millert, and the belly is tinged with much less yellow
so that it looks grayish-green. The edges of the throat are especially
pale, almost white. In all these respects it is almost exactly intermediate
between miilleri and the specimen of Manacus manacus abditivus which I
took at Caucasia. The latter is white wherever miller: is tinged with yel-
low, and shows none of the yellowish tint seen in M. m. flaveolus. Unfor-
tunately I did not get specimens of the bright yellow males at Caucasia,
but I am sure that they were as bright as typical medlerz. In summary,
the hybrid is half way between millert and abditiwus in the amount of
yellow which suffuses the plumage except in the black regions. Date for
my specimens is 21 June 1962” (E. O. Willis, in /z#t.).
Other localities in the Cauca region where manacus and vitellinus come
into contact are Puerto Valdivia (Chapman, 1917; see fig. 5, 2) and
“Remedios.” The village of Remedios is on the eastern slope of the
Central Cordillera facing the Magdalena Valley (fig. 5, 4); Willis has
found here only M. manacus during a two-week visit in 1962. For that
reason it seems probable that the vetellinus specimens taken by T. K.
Salmon during the last century actually came from just across the low
divide of the Central Cordillera (fig. 5, 3). Two other “Remedios” males
of M. manacus abditivus “have the white areas of the plumage very faintly
tinged with yellowish” (Hellmayr, 1929, p. 68) and also may have been
collected west of this village in the possible contact zone with M. vitel-
linus. The bird from Barranca Bermeja (Hacienda Monte Bello) reported
by Borrero and Hernandez (1957) and Borrero, Olivares, and Hernandez
(1962) as “M. vitellinus” is preserved in the Bogota collection; upon re-
determination it proved to be a female of M. manacus abditivus. The humid
middle Magdalena Valley is inhabited exclusively by M. manacus which
comes in contact with M. vitellinus only west of the northern tip of the
Central Cordillera in the lower Cauca region.
A second zone of contact between M. vitellinus and M. manacus is in
the Pacific lowlands of southwestern Colombia and northwestern Ecuador.
Manacus manacus has crossed the Andes in northern Pert and has extended
its range northward into the Pacific lowlands, meeting M. vitellinus at
Guapi (fig. 5, 5) and near Paramba (fig. 5, 6). Olivares (1958) collected
both forms in the environs of Guapi, and Hellmayr (1929, p. 70) de-
scribed an intermediate bird from Paramba which was collected with
normally colored specimens of M. manacus. This bird most probably is a
hybrid. It should be noted that the courtship displays of manacus and
vitellinus are in general identical, with only minor differences (Snow, 1962).
The Central American form candei is not known to be in contact with
1967 HAFFER: COLOMBIAN BIRDS 17
M. vitellinus cerritus of extreme western Panama on the Caribbean slope
(Carriker, 1910; Wetmore, 1959). This, however, seems rather unlikely
and needs confirmation in the field. Eugene Eisenmann wrote (in /itt.), re-
garding the nature of M. vitellinus cerritus: It “is a very variable form
ranging in the same locality (Almirante, Bocas del Toro) from individuals
that in orange yellow color tone are like vitellinus to birds that are nearer
to lemon yellow. To me cerritus suggests the result of some contact of
vitellinus with candet in the past. . . . I believe it most likely that birds
resembling cerritus, rather than true candei, will be found in the Costa
Rican area just west of the Rio Sixaola.”
It is concluded that candei and vitellinus originated as peripheral isolates
of the Amazonian manacus in Caribbean Central America and in the
Chocé Refuge, respectively. Apparently they have not reached full species
status, still replacing each other geographically and hybridizing along
narrow zones of secondary contact. It seems justifiable to speak of a
cande: and vitellinus “group” or of semispecies within the species unit
Manacus manacus (Linnaeus).
GOOD SPECIES
Many trans-Andean forms developed sufficient sexual isolating mecha-
nisms during geographic separation to permit the sympatric occurrence
with the Amazonian parent population upon its re-invasion into the
forest region west of the Andes. If the cis- and trans-Andean allies to-
day still are separated by a distributional gap, their high degree of
morphological difference often indicates that they are specifically distinct.
However, some pairs of such geographically isolated forms are variously
treated by different authors as still being subspecies of a single unit or
as having already reached species status, for example, the following
trans-Andean birds: Laterallus (melanophaius) albigularis, Leucopternis (schis-
tacea) plumbea, Heliothrix (aurita) barroti, Myrmornis (torquata) stictoptera,
Mytobius (barbatus) sulphuretpygius, Myiornis (ecaudatus) atricapillus, Cypho-
rhinus (aradus ) phaeocephalus, Polioptila (guianensis) schistacergula, and Tangara
(nigrocincta) larvata. In each case the specific name of the cis-Andean
relative, which is also the older name, is in parentheses. A future com-
parison of the behavior and habitat patterns of these allies may facilitate
a decision as to their systematic status.
Only a few characteristic examples, of a total of about 100 trans-
Andean species, have been assembled in tables 1-4. The groups dis-
tinguished on the basis of their distribution pattern are briefly discussed
below:
Group A (table 1) comprises trans-Andean species that are restricted
18 AMERICAN MUSEUM NOVITATES NO. 2294
to the Choco region or have extended their ranges into parts of Central
America. In most cases a large gap separates the trans- and cis-Andean
forms; however, Pachyrhamphus cinnamomeus and P. castaneus approach each
other geographically in northwestern Venezuela. It would be interesting
to study both forms in the possible zone of secondary contact. It should
be noted that, in all three species pairs of the cotingid genera Lipaugus,
Rhytipterna, and Laniocera, the trans-Andean representative changed its
general plumage color from the gray of the Amazonian forms to rufous
brown.
Group B (table 2) is composed of trans-Andean species that have
variously differentiated populations both in Central America and in the
Choco region. Some of the Central American forms, all of which orig-
inated in the Caribbean Refuges, are still isolated from the Chocé popu-
lation by a gap in Panama or in northwestern Colombia, or in both
(Galbula through Gymnostinops). This gap may be due to unsuitable eco-
logic conditions or simply lack of sufficient population pressure. The gap
between species pairs in Columba (Oenoenas), Trogon, and Pionopsitta is in
the lower Atrato Valley; between those in Cotinga, in western Panama;
and between those in Gymnostinops, in eastern Panama.
Several Central American forms came into secondary contact with
the Chocé population either in western Panama or in the Uraba region
(Dysithamnus through Cyanerpes). A narrow zone of sympatry seems to
have been found only in Dysithamnus (Eisenmann, 1955; Slud, 1964). In
the remaining cases both trans-Andean forms are either known to hy-
bridize or are assumed likely to do so on the basis of their morphological
similarity and strict geographic replacement. Some of the cis-Andean
representatives in this group are partly sympatric with the trans-Andean
form [Columba (Ocnoenas) subvinacea, Chalybura buffoni|. In other cases a
narrow zone of hybridization is either known to exist (Galbula ruficauda,
Manacus manacus), or its existence seems very probable (Glaucis hirsuta).
Group C (table 3) comprises trans-Andean species without a represen-
tative in the Chocé region. They are restricted to Central America or, in
a few cases, extended their range later into northwestern Colombia.
Group D (table 4), finally, comprises 14 trans-Andean genera; it should
be noted that the generic separation of Allocotopterus and Zarhynchus is
questionable (Hellmayr, 1929, 1937). One genus is restricted to Central
America (not including Chrysothlypis which represents Erythrothlypis), and
five are restricted to the Choco region. Obviously these genera represent
early trans-Andean isolates, of which the Amazonian representatives are,
in most cases, unknown.
Another group of characteristic trans-Andean forest species are the
1967 HAFFER: COLOMBIAN BIRDS 19
TABLE 1
Group A: TRANs-ANDEAN SPECIES RESTRICTED TO THE CHOocé REGION
oR EXTENDING THEIR RANGES INTO CENTRAL AMERICA
(Species not connected by a symbol are separated by a distributional gap.)
Central American Elements Chocé Elements Amazonian Elements
* <—_——_— Leucopternis semiplumbea L. melanops
Bucco noanamae B. tamatia
—————— Nystalus radiatus N. chacuru
Xenerpestes miniosi X. singularis
<—_—————— Mtrospingus cassinii M. oleagineus
-———_—— Malacoptila panamensis M. fusca
<———— M yrmotherula fulvieniris M. leucophthalma
———— ylophylax naevioides HZ. naevia
<——————- Lipaugus unirufus L. vociferans
<——_——— Rhytipterna holerythra R. stmplex
<—————— Laniocera rufescens L. hypopyrrha
<——— Pachyramphus cinnamomeus P. castaneus
<————— Celeus loricatus C. grammicus
“ Chocé elements advancing into Central America.
“Nechi elements” (see above, under Nechi Refuge). They are confined
to northern Colombia, or have occupied additional portions of Panama
or northwestern Venezuela, or both.
CENTRAL AMERICAN ELEMENTS IN NORTHWESTERN
COLOMBIA
During the extension of humid forests after dry climatic periods a
northwardly directed invasion of Chocé elements and cis-Andean forms
was noted in Central America. However, a smaller number of forest
birds also advanced in a southern direction from Middle America into
eastern Panama and northern Colombia. Some met in this area their
west-Colombian or Amazonian representatives, which had been isolated
in the Chocd or Amazonian Refuge, respectively; i.e., Pteroglossus t.
torquatus hybridizes with the Chocé form P. (t.) sanguineus in the Uraba
region and approaches the range of its cis-Andean representative P.
pluricinctus in northwestern Venezuela (fig. 11). Other species advancing
into northwestern Colombia are still separated from their Choco repre-
sentatives by a gap: Pronopsitta haematotis, Trogon m. massena, and Pittasoma
michleri (tables 2 and 4). “True” Central American forms without close
relatives in northwestern Colombia that in part advanced even into the
humid Magdalena Valley include the following (fig. 6): Rhynchortyx cinctus,
Hylomanes momotula, Gymnocichla nudiceps, and Oncostoma cinereigulare. Others
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22 AMERICAN MUSEUM NOVITATES NO. 2294
Fic. 6. How Central American elements
advanced into northwestern Colombia.
Key: Heavy dashes, Rhynchortyx cinctus; fine
dashes, Hylomanes momotula; heavy dots, Oncos-
toma cinereigulare; fine dots, Gymnocichla nudiceps
and Myrmornis torquata (except near Caribbean
coast); fine line, Selenidera spectabilis.
have closely allied forms in the Amazonian forest, such as Selenidera
spectabilis, Deconychura longicauda, Myrmornis (torquata) stictoptera, and Monasa
morphoeus. It should be emphasized that the southward invasion of some
Middle American forms was apparently almost negligible compared to the
main stream of northward-advancing Chocéd and Amazonian elements
during the humid climatic periods of the Pleistocene and post-Pleistocene.
AMAZONIAN ELEMENTS THAT CROSSED THE ANDES IN
NORTHERN PERU
In the high mountain range of the Central Cordillera of the Colom-
bian Andes, there is no pass below 2000 meters which could have per-
mitted an exchange of the cis- and trans-Andean lowland faunas by a
TABLE 3
Group C: Trans-ANDEAN Forms RESTRICTED TO CENTRAL AMERICA OR EXTENDING
THEIR RANGES INTO NORTHWESTERN COLOMBIA
(Species not connected by a symbol are separated by a distributional gap.)
Central American Elements Chocé Elements Amazonian Elements
a
Selenidera spectabilis ——_——_______—_—__+ S. reinwardtit
Deconychura longicauda subsp. ———_______» D. longicauda subsp.
Aratinga finschi A. leucophthalma
Piprites griseiceps P. chloris
“Central American elements advancing into northwestern Colombia.
1967 HAFFER: COLOMBIAN BIRDS 23
TABLE 4
Group D: Trans-ANDEAN GENERA PossiBLy REPRESENTED BY SOME OTHER GENUS
IN AMAZONIA
(Species not connected by a symbol are separated by a distributional gap.)
Central American Elements Chocé Elements Amazonian Elements
Phlogothraupis sanguineus ?
Carpodectes nitidus + C. antoniae C. hopket Xipholena sp.?
Pittasoma michleri P. rufopileatum 2
Bangsta arcaet B. rothschildi Buthraupis sp.?
Heterospingus rubrifrons H. xanthopygius Tachyphonus sp.?
Chrysothlypis chrysomelas Enythrothlypis salmoni Thlypopsis sp.?
Androdon aequatorialis iy
Allocotopterus deliciosus Machaeropterus regulus
Sapayoa aenigma ?
Cercomacra sp.?
Sipia berlepschi }
Sipta rosenbergi
Xenomis setifrons Pygiptila sp.?
@ <—_____________ Phaenostictus mcleannani Phlegopsis sp.
——______—————_ Zarhynchus wagleri Ocyalus lattrostris
4Chocé elements advancing into Central America.
direct crossing of the mountains. The Colombian Andes have been a
highly effective barrier to all lowland forest birds since the beginning of
the Pleistocene. Only a few Chocé species seem to have crossed the
rather low Western Cordillera to occupy the eastwardly adjoining Cauca
Valley (i.e., Manacus vitellinus viridiwventris; fig. 5). The Andalucia pass of
the Eastern Cordillera probably did not serve as a pathway for Amazo-
nian forest birds into the arid upper Magdalena Valley because of eco-
logical reasons (Miller, 1952). Amazonian species advanced exclusively
around the northern tip of the Colombian Andes, following the lowlands
along the Caribbean coast; a direct crossing of the mountains in this
area appears impossible. However, the narrowing Andes to the south seem
to offer several pathways for Amazonian forms to reach the Pacific low-
lands in northern Pert and southern Ecuador. The deeply incised valleys
on each side of the mountain body in this region are mostly dry and
devoid of heavy forest today, but must have been occupied to a large
extent by lowland forest faunas during humid climatic periods of the
past. Chapman (1917, 1926) and Koepcke (1961) have pointed out that
an exchange of cis- and trans-Andean faunas probably took place at
the low Porculla pass (2150 meters) in northern Pert (“Marafion route’’).
Chapman (1923) also discussed the possibility of a “Loja route” in south-
24 AMERICAN MUSEUM NOVITATES NO. 2294
ern Ecuador. It seems very reasonable to assume that during humid
periods certain Amazonian species “spilled over” to the west following
various low passes in the narrow Andes of southern Ecuador and north-
ern Perd. Particularly interesting examples are found in the 77ogon mela-
nurus group (fig. 15), in Formicarius nigricapillus, and in Manacus manacus
(fig. 5) (Chapman, 1926, pp. 411, 536). The following west-Ecuadorian
forms probably originated from small founder populations that crossed
the Andes in this region:
Sittasomus griseicapillus aequatorialis
Pachyrhamphus spodiurus
Cacicus cela flavocrissus
Others have extended their range northward into the Choco region,
or in some cases even into Central America:
Crax rubra
Osculatia saphirina purpurata
Attila cinnamomeus torridus
Micromonacha lanceolata
Pipra mentalis
Gymnopithys leucaspis
Thamnistes anabatinus
Microrhopias quixensis
These species either have their closest relatives in the upper Amazonian
lowlands rather than in Venezuela, for example, Crax globulosa, Osculatia
s. Saphirina, Pipra chloromeros, or the cis-Andean population is restricted to
the central and southern part of the Amazonian forest.
DISCUSSION
The amazing concentration of endemic forms in the forested lowlands
west of the Andes is explained by the following facts: (1). Relatively
small populations of Amazonian forest birds were repeatedly isolated in
forest refuges west of the Andes during Pleistocene and post-Pleistocene
periods of drought which broke forest connections and allowed the de-
velopment of differences by selection and chance. (2). The repeated
restoration of connection between the lowland forests west and east of
the Andes during humid climatic periods allowed an increasing num-
ber of small Amazonian founder populations! to reach the forests west
of the Andes in Central America and western Colombia. This led to a
1 These founder populations contained “inevitably only a small fraction of the total
variation of the parental species” (Mayr, 1963, p. 529). This was also of great importance
for the rapid deviation of a trans-Andean form from its cis-Andean parent species (Mayr’s
“founder principle”).
1967 HAFFER: COLOMBIAN BIRDS 25
gradual accumulation of endemic trans-Andean forms. These are of very
different age and have reached today various stages of taxonomic differ-
entiation. (3). Owing to the repeated establishment of forest connections
during humid periods, multiple invasions of the same Amazonian popula-
tion into the region west of the Andes occurred in several cases.
The uplift of the northern Andes to their present height led to the
formation of a very effective barrier to the lowland faunas on either side
of the mountains. However, this event was only the indirect cause of the
development of the numerous trans-Andean species. The direct cause was
the repeated change of dry and wet climatic periods during the Pleisto-
cene and post-Pleistocene which resulted in a corresponding reduction
and expansion of the tropical lowland forests. Similar conclusions have
been reached by other authors regarding different parts of the tropics
(Stresemann and Grote, 1929; Stresemann, 1939; Darlington, 1957, p.
587; Keast, 1961; Mayr, 1963, p. 372; Moreau, 1963; Hall, 1963).
The above interpretation of the faunal differentiation west of the
Andes contrasts sharply with Chapman’s theory (1917, 1926). He assumed
that part of a “pre-Andean” fauna was cut off west of the Andes by
the rising mountain ranges of the northern Andes. However, the existence
of a “pre-Andean” lowland fauna west of the Andes seems to me most
unlikely, since these lowlands were covered by shallow seas before the
uplift of the mountains. Island faunas existed on archipelagoes in the
region of Middle America, but these permitted only a restricted immigra-
tion of Amazonian forms. The low cordilleras themselves were also
separated from the Amazonian forest by shallow seas until the begin-
ning of the Pleistocene. Moreover the separation of the lowlands, east
and west of the Andes, by the Andean uplift was not complete; both
regions remained narrowly connected north of the mountain ranges in
northern Colombia and northwestern Venezuela, and a frequent exchange
of the cis- and trans-Andean faunas was possible through Caribbean
lowlands. ‘These facts seem incompatible with Chapman’s theory. Griscom
(1932, 1935) in addition assumed that the Pleistocene refrigeration had
forced the Central American lowland fauna to retreat southward into
western Colombia, thus leading to the surprising concentration of endemic
forms in the Choco region. However, it is shown above that the temper-
ature depression of the Pleistocene most probably did not affect the
tropical lowland fauna of the central and southern part of Middle
America.
Nevertheless the close relationship of the “Colombian Pacific fauna”’
and the Central American fauna stressed by Chapman (1926) remains
a zoogeographic fact. It seems best explained by an intensive faunal ex-
26 AMERICAN MUSEUM NOVITATES NO. 2294
change that took place between both regions during the humid periods.
For that reason it appears useful to combine them in a zoogeographic
classification as was done by Hershkovitz (1958). This author correctly
interpreted the west-Colombian lowlands as the “South American root”
of his Middle American province. The centers of the forest faunas of this
Middle American province are represented by the former Caribbean
Central American Refuges and the Pacific Chiriqui Refuge as well as
the Chocd and Nechi refuges of Colombia.
A problem of particular interest is the age of the bird speciation west
of the Andes. The range extensions that led to “allopatric” hybridization
in western Panama and in the Uraba region are probably of very recent
age and may be only several thousand years old. However, we do not
know for how long the hybridizing allies had been isolated. In cases
such as Glaucis (hirsuta) aenea, Galbula (ruficauda) melanogenia, and Formi-
cartus nigricapillus, in which the isolated west-Colombian and Central
American populations are not even subspecifically distinct, the separation
appears to be very recent and of post-Pleistocene age. However, in most
other trans-Andean species no decision as to a Pleistocene or post-
Pleistocene age can be made, although it seems reasonable to assume
that more strongly differentiated genera! and species already had orig-
inated in early Pleistocene time.
In an excellently illustrated article on the morphology and distribution
of the butterfly genus Hel:conius, Emsley (1965) related the differentiation
of this group of neotropical insects to the Tertiary paleogeographic his-
tory of northwestern South America. He was silent, however, about
Pleistocene climatic changes and their possible effect on the distribution
of the various species studied. I would assume that these climatic changes
were equally important for the distribution of butterflies as they have
been for that of birds. For this reason some of the speciation phenomena
described by Emsley (1965) are perhaps better explained by the climatic,
rather than the paleogeographic, history of the recent geologic past, par-
ticularly for the differentiation of some of the endemic species inhabiting
the lowlands north and west of the Andes. Nevertheless, a few trans-
Andean endemics in butterflies and birds may have originated on the
isolated islands of the emerging northern Andes during middle and late
Tertiary time and later extended their ranges onto the emerging low-
lands west and north of the rising mountain chains. I assume, however,
that the great majority of the forest species, inhabiting today the trans-
Andean lowlands, advanced into these regions after the final connection
1 These are mostly monotypic and nothing but strongly differentiated geographical
isolates,
1967 HAFFER: COLOMBIAN BIRDS 27
with the Amazonian lowlands was established at the end of Tertiary
time and when dense forests developed around the rising mountain
ranges. The differentiation of these trans-Andean populations was then
related mainly to the Pleistocene climatic history of northern South
America and of Middle America rather than to the Tertiary orogenic
development of the northern Andes. On the other hand, the differentia-
tion of the numerous Amazonian species of butterflies and birds did
probably start earlier in the Tertiary and was influenced by the paleo-
geographic history of these areas, as well as by the Pleistocene climatic
changes.
ALLOPATRIC HYBRIDIZATION AT THE NORTHERN MARGIN
OF THE CHOCO REFUGE
When the forests of Central America and northwestern Colombia were
united after a sub-Recent period of drought, previously isolated bird
populations came into secondary contact as long as they followed the
extending forests. Zones of allopatric hybridization resulted close to the
eastern margin of the Caribbean Costa Rica Refuge and at the northern
margin of the Choco Refuge (fig. 4). For this reason the forests of Carib-
bean western Panama and of the Uraba region of northwestern Colombia
are of particular zoogeographic importance. Both areas have been treated
in special publications (Peters, 1931; Eisenmann, 1957; Haffer, 1959),
but no details of the secondary contact zone of any of the allopatric
“species” pairs of these regions are known, except for the hybridization of
Chalybura (urochrysia) melanorrhoa and C. u. isaurae in western Panama
(Eisenmann and Howell, 1962).1
Pteroglossus torquatus torquatus AND Pteroglossus
(torquatus) sanguineus
The Collared Aragari (Pteroglossus torquatus) of Central America and
northwestern South America is replaced in the Pacific lowlands of Colom-
bia by the Stripe-billed Aragari (P. sanguineus). On the basis of marked
differences in the coloration of the bill and hind neck, both forms were
considered to be specifically distinct. However, they had never been
found living in the same area. For this reason I collected material and
made observations in the Uraba region, where they meet, to find out their
relationship and taxonomic status.
1 The distribution and interrelationship of Crax rubra and C. alberti, Pipra mentalis and
P. erythrocephala, Rhynchocyclus brevirostris and R. olivaceus are discussed in a separate article
(Haffer, in press, c). The allies of these pairs probably have reached species status and
replace each other geographically on account of ecologic competition.
28 AMERICAN MUSEUM NOVITATES NO. 2294
Both forms are similar in habits and coloration (fig. 10). Sanguzneus is
only slightly larger, and differs from torquatus in having a yellow tip to
the bill, a black stripe along the upper mandible, and in lacking a chest-
nut band across the hind neck, which is characteristic of torquatus. The
bill of the latter has a black tip and no black stripe. The neck band of
torquatus from northern Colombia is light chestnut in males and dark
maroon in females. Both “species” can be observed in the early morning
Fic. 7. Distribution of Pteroglossus torquatus and Pteroglossus (torquatus) san-
guineus in the Uraba region, northwestern Colombia. Elevations over 300 meters
are in black. The framed area east of the Gulf of Uraba is shown in more de-
tail in the right-hand map. See text for numbered localities.
Key: Horizontal lines and quadrangles, Pteroglossus torquatus torquatus: vertical
lines and circles, Pteroglossus (torquatus ) sanguineus; heavy dots, hybrid zone (H).
and late afternoon in small groups of from five to 20 individuals along
the river valleys in forested regions. Skutch (1958) described the habits
of P. torquatus and of P. (torquatus) frantzii, a form closely allied to P.
torquatus restricted to the Pacific coast of Costa Rica and western Panama,
which possesses a differently colored bill.
The distribution, as mapped in figure 7, is as follows:
EasT OF THE GULF OF URaBA: The area of the upper Rio Sint is in-
habited by torquatus (de Schauensee, 1950). To the west I have collected
17 specimens of this form in the valley of the Rio Mulatos. These birds
are typical for torquatus; they have the tip of the bill black and no stripe
1967 HAFFER: COLOMBIAN BIRDS 29
on the upper mandible. The light (male) or dark (female) chestnut neck
band is seen in all specimens, although narrow and not complete in
three adult males. The rather small size of the Mulatos birds is also
typical for torquatus (10 males: wing, 145.1; tail, 158.2; bill, 99.9 mm.).
Pteroglossus sanguineus inhabits the valleys at the western foot of the
Serrania de Abibe (Rio Imamad6, Chigorodd, Carepa) and ranges north
to the region of the Rio Currulao, Rio Guadualito, and Turbo (Haffer,
1959).
WEST OF THE GULF OF URABA: Torquatus is known in eastern Panama
from Cana (Griscom, 1929) and from the Rio Jesusito (Bangs and Bar-
bour, 1922). Wetmore (zn litt.) has collected typical specimens of this
form at Jaqué and Armila. The only bird taken on the Colombian side
is from the Rio Tanela (Haffer, 1959). Sanguineus is a common bird from
about the Panamanian border of Colombia southward.
In more detail (as numbered on the map, fig. 7) the localities from
which the two forms have been recorded are as follows:
Pteroglossus (torquatus) sanguineus: 1, Rio Napipi (commonly observed); 2, Rio
Truando (de Schauensee, 1948-1952); 3, Jurad6 (one male, Bogota, de Schauen-
see, 1948-1952) and upper Rio Juradé between mouth of Rio Jampavadé and
Rio Antadé (seven males, five females); 4, Rio Salaqui (de Schauensee, 1948-
1952); 5, Sautata (one male, one male hybrid); 6, Alto Bonito (Chapman, 1917);
7, Pavarandocito (two males, one female); 8, Rio Imamad6 (one male, one fe-
male); 9, Rio Chigorodé (five females); 10, Rio Carepa, 2 kilometers above
mouth of Sucia Creek (five males, four females); 11, Rio Currulao at Turbo
road (one male, one female); 12, Rio Currulao, mouth of Tia Lopez Creek (one
female); 13, Rio Currulao, mouth of Limén Creek (one male); 14, Rio Gua-
dualito (one male, one female); 15, Turbo (one female).
Hybrid Zone: 5, Sautata (two males); 16, Rio Cope (11 males, nine females).
Pteroglossus torquatus torquatus: 17, Rio Mulatos, mouth of Umbito Creek (one
male); 18, Rio Mulatos, camp II (eight males, four females); 19, Rio Mulatos,
camp III (two males, two females); 20, Alto de Quimari (14 specimens, de
Schauensee, 1950); 21, Tierra Alta (three specimens, de Schauensee, 1950);
22, Murucuct (three specimens, de Schauensee, 1950); 23, Rio Tanela (one
male, Haffer, 1959); 24, Armila (Wetmore, in litt.); 25, Cana (Griscom, 1929);
26, Rio Jesusito (Bangs and Barbour, 1922); 27, Jaqué (Wetmore, in /itt.).
HYBRIDIZATION
While mapping the ranges of both strictly allopatric forms in the
Uraba area, I found a hybrid population at the middle course of the
small Cope River 8 kilometers north of Turbo in April, 1964 (fig. 7, 16).
I collected 20 specimens (11 males, nine females) of this population in
the immediate surroundings of our camp. These birds represent every
conceivable stage between the torquatus and sanguineus extremes and show
beyond doubt that both forms hybridize freely where they meet.
30 AMERICAN MUSEUM NOVITATES NO. 2294
To facilitate the color analysis of the hybrids the hybrid-index system
was applied. This method has been used frequently in recent years (Sibley
and Short, 1959, 1964; Sibley and Sibley, 1964; Short, 1965) and re-
quires no further description.
The index values for color characters of Pteroglossus forms are as
follows:
Band across hind neck
0, missing, as from sanguineus
1, barely indicated
2, half developed
3, almost complete
4, complete, as in torquatus
Stripe along upper mandible
0, complete, as in sanguineus
1, almost complete
2, half developed
3, weakly developed
4, missing, as from torquatus
Tip of upper mandible
0, yellow, as in sanguineus
1, pale yellow
2, mixed yellowish and blackish
3, blackish
4, black, as in torquatus
The values for these characters are determined and totaled to give
the hybrid index of each hybrid specimen. Pure torquatus specimens have
the value 12, hybrids have indices of from 1 to 11, and pure sanguineus
specimens have the value 0.
The histogram of the hybrid indices (fig. 8) shows the intermediate
position of the Rio Cope population between torquatus and sanguzneus. It
bridges the morphological gap between these forms almost completely.
In total it is slightly closer to sanguineus, since the mean hybrid index is
only 4.7 and the measurements also agree with those of the larger Chocd
form (table 5). In each character every stage between the torquatus and
sanguineus extremes and every conceivable combination of these character
stages are represented in the hybrid series. There are specimens with an
almost pure bill of torquatus but without any indication of the chestnut
band across the hind neck. Other specimens display a combination of an
almost complete chestnut band with the pure bill of sanguzneus. These
numerous intermediate types indicate that the hybrids are fertile and
that free crossing and backcrossing occur. It should be noted that pure
parental types are lacking in the sample obtained.
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32 AMERICAN MUSEUM NOVITATES NO. 2294
OCCURRENCE OF A HYBRID ZONE
Figure 7
A hybrid population was developed only when a sanguineus population
and a ¢orquatus population met without any orographic barrier. Contrary
to my expectation, relatively low mountain ranges of from 300 to 500
meters in elevation prevent virtually any gene flow.
~ |5
f@)
torquatus —————>
Rio Mulatos
5
0)
S 5
“Ys Y 5 Rio Cope
YUMUOUMWEDY
15
road
10
<——— sanguineus south of
Turbo
5
Hybrid- Index
012345 678 9 10 II l2
Fic. 8. Histogram of the hybrid indices of the Rio Cope population of
Pteroglossus. Number of specimens is indicated at left and right, respectively.
East OF THE GuLF OF UrasA: The boundary of the ranges of both
forms in this region is the divide of the rivers flowing west toward the
Gulf and north to the Caribbean Sea, respectively. The watershed is
formed in this area by chains of narrow, steep mountains that range in
elevation from 300 to 700 meters. Acting as a highly effective barrier,
they apparently prevent any visible gene flow, shown by the spatial
proximity of a pure sanguineus population in the upper Carepa and Cur-
Fic. 9. Pteroglossus torquatus torquatus (top figure) and Pteroglossus (torquatus)
sanguineus (bottom figure), with four hybrids from the Rio Cope (H-0281,
0280, 0271, 0270). Observe, from top to bottom, the disappearance of the
chestnut collar across the hind neck; the replacement of the black tip of the
bill by a yellow one; the development of a black stripe along the upper man-
dible; and the blackening of the red skin in front of the eye.
34 AMERICAN MUSEUM NOVITATES NO. 2294
rulao valleys and of a pure torquatus population in the neighbouring
Mulatos Valley far up the headwaters. The lack of hybridization in this
area has no biological implications and may be entirely due to isolation
by the mountains. The whole region is uniformly covered with “Moist
Tropical Forest” (Espinal and Montenegro, 1963) that has been cleared
around Turbo and along some of the major rivers. In three torquatus
specimens of a total of 12 collected at camp II on the Rio Mulatos, the
chestnut band across the hind neck is not quite completely developed.
This fact may indicate a slight introgression of some sanguzneus genes of
the Currulao population across the divide which is here rather low; how-
ever, this must be confirmed by more material from this area.
Pteroglossus torquatus met the northward-advancing sanguineus just north
of Turbo. The hybridization of both populations was not impeded in
this area by the north-south mountain chains. Here both forms met in
the intervening valleys and hybridized freely. Besides the Rio Cope area,
further intergradation of these Aragari toucans probably takes place in
the valleys of the Los Indios Creek and Turbo River. Unfortunately I
did not find either form on a three-day trip along the Rio Turbo.
WEsT OF THE GULF OF URaBA: One of the two adult males that I
collected at Sautata on the lower Atrato River in 1959 is a hybrid with
the hybrid index of 4. In this specimen the stripe of the upper mandible
is only weakly developed and the tip of the bill is very pale yellow;
there is no indication of a neck band. Another hybrid specimen was
collected “near Jurado” and was mentioned by de Schauensee (1950)
under torquatus. In this female, the “bill shows a rudimentary black stripe
on the side of the upper mandible” (de Schauensee, in /:tt.). Probably
it was collected some distance north of the village of Juradé in the head-
waters of the Rio Jampavad6é or Rio Juradé where both forms meet.
All 12 specimens (seven males, five females) that I collected near the
mouth of the Rio Jampavad6 (at the Rio Juradd) in March, 1965, are
pure sanguzneus, as is a single male from “Jurad6” in the Bogota collections
(collector K. von Sneidern, 1949). As well as the secondary intergradation
of both forms in the upper Rio Juradé and in the Sautata area, other
small and restricted hybrid populations are probably to be found in the
headwaters of the Tuira River along the Panamanian/Colombian
boundary.
A very narrow hybrid zone is indicated by the highly variable Rio
Cope population and by the abrupt transition into a pure sanguineus
population along the Turbo road. Probably the width is less than 20
kilometers.
1967 HAFFER: COLOMBIAN BIRDS 35
Fic. 10. Forms of Pteroglossus from northwestern South America. From top
to bottom: Pteroglossus castanotis, P. pluricinctus, P. (torquatus) sanguineus, and P.
torquatus.
CONCLUSIONS
1. No sufficient sexual isolating mechanisms have been developed dur-
ing the geographic separation in Caribbean Central America (torgquatus)
and in the Chocd Refuge (sanguineus) to prevent free interbreeding of
both forms where they meet today.
2. The occurrence of a hybrid zone is not correlated with ecological
factors but depends strongly on orographic conditions.
3. The forms sanguineus and frantzii1 are considered as semispecies
within the species unit Pteroglossus torquatus.
4. The trans-Andean species Pteroglossus torquatus is subdivided in the
following manner:
torquatus group: Pteroglossus torquatus erythrozonus, Pteroglossus torquatus torquatus,
and Pteroglossus torquatus nuchalis
1This form of the Pacific slope of southern Central America probably meets torquatus
in the Aguacate Mountains of Costa Rica (Slud, 1964).
36 AMERICAN MUSEUM NOVITATES NO. 2294
frantzii group: Pteroglossus (torquatus) frantziu
Sanguineus group: Pteroglossus (torquatus) sanguineus and Pteroglossus (torquatus )
erythropygius
THE Pteroglossus pluricinctus SUPERSPECIES
Pteroglossus torquatus is the only trans-Andean member of the Ama-
zonian genus Pteroglossus that ranges northward to Mexico and eastward
to northern Venezuela. Its nearest cis-Andean representative is Ptero-
glossus pluricinctus which has a whitish upper mandible, black head, throat,
P. (t) trantzii” ;
P. (t)songuineus-Group
P. pluricinctus
60°w. Gr.
Fic. 11. Distribution of the Pteroglossus pluricinctus superspecies.
and breast, and a mixed black and red band across the upper abdomen;
it is also similar in size and proportions (table 5). Pteroglossus castanotis
is more distantly related, as shown by its different coloration and pro-
portions (fig. 10). It seems justifiable to combine Pteroglossus pluricinctus
and the trans-Andean forms of Pteroglossus torquatus into one superspecies.
Both species approach each other closely in western Venezuela but re-
main separated by the dry area around Barquisimeto. Pteroglossus torquatus
possibly originated from proto-fluricinctus stock that advanced into the
trans-Andean region during one of the early humid periods and was
isolated later in the Caribbean Central American Refuges (torquatus), in
the Chiriqui Refuge (/rantzit), and in the Chocd Refuge (sanguineus),
respectively.
1967 HAFFER: COLOMBIAN BIRDS 37
Fic. 12. Distribution of Galbula ruficauda ruficauda and Galbula (ruficauda)
melanogenia in the Uraba region, northwestern Colombia. Elevations over 400
meters are in black. The framed area east of the Gulf of Uraba is shown in more
detail in the right-hand map. See text for numbered localities.
Key: Galbula r. ruficauda, hatched horizontally and quadrangles; Galbula (r.)
melanogenia, hatched vertically and circles; hybrid zones (H), dotted.
Galbula ruficauda ruficauda AND Galbula (ruficauda) melanogenia
The Rufous-tailed Jacamar (Galbula ruficauda) is a common neotropical
bird that ranges from southern Brazil to Mexico. The trans-Andean form
melanogenia inhabits tropical Middle America (except El Salvador) to
western Panama (Eisenmann, 1955) and the Pacific lowlands of Colom-
bia and northern Ecuador. A peculiar hiatus in its range occurs through-
out eastern and central Panama where no individual of Galbula has ever
been found (Griscom, 1935; Wetmore, zn litt.; Eisenmann, in lit.).
The distribution in northwestern Colombia is mapped in figure 12,
and the detailed records coincide with the numbers on the map, as
follows:
Galbula (ruficauda) melanogenia: 1, Upper Rio Napipi (four males, one female);
2, Rio Truandé (five males, three females); 3, Juradéd (de Schauensee, 1948-
1952); 4, upper Rio Juradé (one male); 5, upper Rio Salaqui at mouth of Rio
Jurachira (one male, one female); 6, Rio Murri (1 female); 7, Frontino (T. K.
Salmon collected a specimen of Galbula at this locality during the last century,
which is cited in the literature under ruficauda; however, the Sucio Valley has
38 AMERICAN MUSEUM NOVITATES NO. 2294
TABLE 6
Co tor DIFFERENCES OF THE TRANS-ANDEAN AND
Cis-ANDEAN Forms oF Galbula ruficauda
G. (1.) melanogenia G. 7. ruficauda
Throat Clear white, chin dusky White tinged with buffy, es-
pecially toward chin
Tail First and second pair green, First pair green, second pair
rest rufous rufous, with only basal part
of outer vane green, rest
rufous
Tail and Relatively short Relatively long
bill
access only to the Atrato plains inhabited by melanogenia, so the bird is almost
surely melanogenia); 8, Alto Bonito (Chapman, 1917); 9, Pavarandocito (one
male); 10, Rio Imamad6 (one male).
Hybrid Zone (H): 11, Rio Chigorodd (one male, one female, one female
juvenile); 12, Rio Carepa, 1 kilometer above mouth of Piedras Blancas Creek
(one male, one female); 13, upper Rio Currulao, at mouth of Ahullamita Creek
(one male); 14, Rio Mulatos, camp III (two males, two females).
Galbula ruficauda ruficauda: 15, Rio Mulatos, camp II (four males, two females);
16, Rio Mulatos, camp I (four males, five females); 17, Alto de Quimari (four
males, three females, de Schauensee, 1950); 18, Rio San Juan (two females);
19, Rio Currulao at mouth of Tia Lopez Creek (two males, two females); 20,
Rio Apartad6 (three males, one female); 21, Rio Guadualito (two males, three
females); 22, Rio Cope (two males, one female); 23, Tierra Alta (one male,
one female, de Schauensee, 1950); 24, Frasquillo (one female); 25, Sautata
(one male, one female); 26, Riosucio (two males, 1 female juvenile); 27, Rio
Salaqui (one male).
During the last century ruficauda has been reported from the Rio
Nercua, the northern headwater of the Rio Truandé (Cassin, 1860).
This determination seems doubtful, however, since I have collected
melanogema along the Rio Truando and at the upper Rio Salaqui to the
north of the Nercua River. Unfortunately Cassin’s Nercua specimen can-
not be found in the collections of the Academy of Natural Sciences of
Philadelphia (de Schauensee, in /itt.; see also Haffer, in press, a, for a dis-
cussion of this record and other doubtful ones from the lower Atrato
Valley).
The ecological requirements of G. 7. ruficauda and melanogenia are simi-
lar, although minor differences are noted. They live along shaded rivers
and creeks in the tropical lowlands and nest in long tunnels which they
excavate in soft banks (see the excellent life-history study by Skutch,
1963). Melanogenia requires a very humid climate in the Chocé region
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40 AMERICAN MUSEUM NOVITATES NO. 2294
and avoids the area with less than 3500 mm. of rainfall per year at the
Gulf of Uraba. It is more confined to forest streams than ruficauda, occu-
pying the overgrown forest border along the riverbanks and disappearing
from an area once the forest has been cut. On the other hand, rujficauda
is commonly found in secondary growth of Calathaea and bamboo in
much-deforested and rather densely inhabited regions with less excessive
rainfall. This ecologic difference is also apparent from the regional dis-
tribution pattern of ruficauda, which avoids the humid center of the
Amazonian forest region. However, in Central America melanogenia ap-
parently also inhabits second growth in only partially wooded areas
(Slud, 1964).
HYBRIDIZATION
Long series of ruficauda (40 specimens) and melanogenia (21 specimens)
from the Uraba region show that both forms differ in coloration and
size consistently. A small and restricted hybrid population was found
only in a few valleys southeast of Turbo. The hybrid specimens col-
lected along the Rio Chigorodé, Carepa, Currulao, and Mulatos are
proof of a limited gene flow between the two forms.
Rio Cuicoropé: One male (wing, 82; tail, 99; bill, 46.2 mm.), one
female (wing, 82; tail, 89.5; bill, 44.5 mm.), one female juvenile. Meas-
urements and color of chin and throat are typical for melanogenia. How-
ever, the inner vane of the second right tail feather of the male is
extensively rufous, and the left second tail feather shows a rufous shaft
streak. Also in the female a narrow rufous shaft streak is seen in the
second pair of the tail feathers. This partial rufous coloring of the shiny
green second tail feathers was never observed in any pure melanogenia
specimen and suggests a definite introgression of ruficauda genes. The
juvenile bird has a black chin and four of the central tail feathers are
green; these are growing and are still too short (about 15 mm. long) to
be checked for hybrid characters.
Rio Carepa: One male (wing, 83; tail, 114; bill, 49 mm.), one female
(wing, 79.5; tail, 91.5; bill, 45 mm.). This pair was apparently mated;
it was collected near the mouth of the Piedras Blancas Creek. It is
interesting to note that the female is melanogenia (the inconspicuous
black chin may show a slight ruficauda influence), whereas the male
phenotypically is a pure ruficauda with a few dark tips to the chin
feathers. This bird apparently belongs to the ruficauda population inhab-
iting the rivers to the northwest of the Carepa locality. Unfortunately
I did not find any jacamars in the north-south upper Carepa Valley,
the original Galbula population of which was probably closer to melano-
1967 HAFFER: COLOMBIAN BIRDS 41
genia. This genus must have left the area when the valley floor was de-
forested some 10 years ago.
Upper Rio CurruLAao aT MouTH OF AHULLAMITA CREEK: One male
(wing, 80; tail, 102; bill, 48 mm.). In coloration of tail and in measure-
ments this bird is intermediate; the color of chin and throat is of the
ruficauda type. The rufous second tail feathers are extensively shiny green
on the outer vane and on the distal portion of the inner vane. This
specimen indicates that the population of the upper Currulao south of
the mouth of Ahullamita Creek is intermediate between both forms.
Upper Rio Mutatos, Camp III: Two males (wing, 84, 82; bill, 50.5
mm.), two females (wing, 78.5, 77; tail, 100, 94; bill, 47 mm.). In colora-
tion these birds are close to ruficauda; however, the chin is slightly dusky
and the measurements are intermediate.
“Quimar?”: A female of melanogenia (wing, 78.5; tail, 95.5; bill, 44.5
mm.) labeled “Quimari” is included in the collections of the Instituto
de Ciencias Naturales, Bogota (No. 8461). It shows a slight ruficauda in-
fluence by a weakly pronounced, dusky chin color. Mt. Quimari is sit-
uated due east of Turbo and is less than 600 meters high. Seven ruficauda
specimens have been reported from this locality by de Schauensee (1950).
These were collected by hunters of von Sneidern, probably in the general
area of “Quimari.” The above female belonged to the same von Sneidern
collection and was presumably taken some distance south of Quimari
in the hybrid zone between ruficauda and melanogenia.
The hybrid populations southeast of Turbo occupy a very narrow area
of approximately 40 kilometers from north to south comprising the val-
leys of the upper Chigorodé, Carepa, Mulatos, and Currulao rivers. The
Serrania de Pavo (700 meters in elevation) just west of the Currulao
and Carepa headwaters prevents any melanogenia influence on the pure
ruficauda population along the Turbo road.
In the lower Atrato region pure ruficauda specimens have been taken
at three different localities (Sautata, Riosucio, lower Rio Salaquf). A
very local hybrid zone may be found between the lower Salaqui and
Truandé rivers. The birds taken along the upper Salaqui are pure
melanogenia. ‘This population is separated from ruficauda at the lower
Salaqui by the steep and rugged Serrania de los Saltos and the narrow
rocky canyon of the Salaqui River itself; probably no gene flow occurs
along this river valley.
CONCLUSIONS
The northern limit of the range of melanogenia in the Chocé region
more or less coincides with the 3500-mm. isohyet. It is here that ruficauda
42 AMERICAN MUSEUM NOVITATES NO. 2294
hybridizes with the trans-Andean bird, forming very restricted and vari-
able hybrid populations. For this reason melanogenia should be considered
as a semispecies within the species unit Galbula ruficauda which is sub-
divided taxonomically as follows:
ruficauda group: Galbula ruficauda ruficauda, Galbula ruficauda brevirostris, and Galbula
ruficauda pallens
melanogenia group: Galbula (ruficauda) melanogenia
rufoviridis group: Galbula (ruficauda) rufoviridis and Galbula (ruficauda) heterogyna
The range of the trans-Andean form melanogenia was presumably inter-
rupted in Panama and in the northern Chocé region during a period of
drought in the recent past. Upon the return of more humid climatic
conditions this gap was only partly closed, for our bird has never been
taken in central or eastern Panama (Griscom, 1935; Wetmore, in litt.).
At the same time the Amazonian form occupied northern Colombia and
the area around the Gulf of Uraba, which was left uninhabited by
melanogenia because of ecological reasons.
Discussion
The zones of allopatric hybridization at the northern margin of the
former Chocéd Refuge are characterized by very narrow width, great
age, and an ecologically quite uniform environment.
THe Narrow Wiptu: On the basis of the data known in Preroglossus
and Galbula the hybrid zones are not broader than 20 to 40 kilometers.
It must be assumed that hybrids are strongly selected against within
the range of each ally. Possibly the small regional extent of the contact
zones prevents, in these cases, widespread swamping despite the lack of
isolating mechanisms (Short, 1965, p. 419).
Tue Great Ace: The hybridization in the Uraba area was caused by
natural range extensions of the allies, which occurred at least several
thousand years ago. It has not been effectively influenced by any human
activity in this region during the last few centuries.
THE ENVIRONMENT: A conspicuous climatic gradient is noted in the
Uraba region by the increase of rainfall as one goes south. However,
this gradient is not steep enough to account for the abrupt geographic
replacement of the birds studied. Only the northern limit in the Chocé
region of the range of Galbula (r.) melanogenia may also correspond with
the ecologic limit of this population. Galbula r. ruficauda, as well as the
Pteroglossus and Manacus forms, very probably would occupy at least part
of the ally’s range were it not for its presence across the zone of contact.
The Pteroglossus and Manacus forms hybridize where they met on the re-
1967 HAFFER: COLOMBIAN BIRDS 43
turn of sufficient forest growth in northern Colombia. In these cases the
position of the hybrid zones changed probably very little since the time
the allies came in contact. In other cases the shifting of the hybrid zone
may have been more pronounced to achieve the present ecologically
balanced situation.
It seems probable that similar cases of hybridization will be found
when the contact zone of other “species” pairs are studied in more de-
tail. The above examples show that large series from the critical area
of geographic replacement and extensive field experience are needed for
a correct evaluation of the relationship of closely related allopatric
forms.
The hybridizations of the Uraba region appear to be comparable to
the situation in the Carrion Crow (Corvus corone) of western Europe
(Meise, 1928). They differ greatly, however, from those cases of narrow
hybrid zones that are found along sharp ecological breaks such as rain
forest and savanna (for examples, see Mayr, 1963). On the other hand,
certain broad hybrid zones studied in the central part of the United
States, in Mexico, and west of Cali, Colombia, by Sibley (Sibley and
Short, 1959, 1964; Sibley and Sibley, 1964; Sibley, 1958) seem largely
due to the recent activity of man, who provided artificial pathways for
the dispersal of previously isolated, closely allied forms.
In a recent paper Bigelow (1965) criticized the emphasis on inter-
breeding in Mayr’s species definition as opposed to “reproductive iso-
lation,” and redefined that term. Bigelow’s modified species definition
(which is intended to turn on the extent of gene flow) led him to con-
sider as “good species” some forms that Mayr (1963) called “semispecies,”
or “subspecies” of a single species. If we followed Bigelow, the forms of
Pteroglossus and Galbula here discussed would have to be considered as
“reproductively isolated” entities (=species) because of the very narrow
width of the hybrid zone. Unfortunately Bigelow did not discuss “semi-
species,” a very useful concept, which includes all transitional cases
between two closely allied populations that are neither good sympatric
species nor broadly intergrading subspecies. I feel that essentially allo-
patric forms that hybridize freely, even along a narrow zone only, should
be distinguished nomenclaturally from good species living side by side.
The semispecies concept of Mayr (1940), as subsequently emended by
Lorkovié (1958), appears to serve this purpose very well.
MULTIPLE INVASIONS INTO THE TRANS-ANDEAN
REGION
Owing to the fact that the cis- and trans-Andean forests became re-
44 AMERICAN MUSEUM NOVITATES NO, 2294
peatedly connected during several humid periods, in a few cases the
same Amazonian species was able to advance more than once into the
lowlands west of the Andes. Such an advance led to the sympatric occur-
rence of the two consecutive invasions, if the first had already developed
a sufficient number of sexual isolating mechanisms. The importance of
multiple invasions for speciation, especially on islands and _ isolated
mountain massifs, has been known for a long time (Stresemann, 1927-
1934; Mayr, 1942, 1963).
Fic. 13. Distribution of the Co-
lumba (Oenoenas) subvinacea species
group. Recently the author has col-
lected C. goodsoni at the northern end
Sar eT of the Western Andes, southeast of
—__—_———————}_~Ss the Gulf of Uraba.
DouBLE INVASIONS
PIGEONS OF THE Columba (Oenoenas) Species GROUP
Figure 13
The Oenoenas group has been treated as a subgenus of Columba but
was recently given generic status by Johnston (1962). Oenoenas plumbea
and Oenoenas subvinacea are distributed over large areas of tropical South
America. Only the latter form advances northward into the highlands
of Costa Rica. Oenoenas nigrirostris and Oenoenas goodsoni are members of
a superspecies and occupy small peripheral areas in Central America and
western Colombia, respectively. Both are believed to be closer to Oenoenas
subvinacea than to Oecnoenas plumbea, mainly on the basis of the general
body color and the cinnamon inner vanes of the primaries. A first inva-
sion of proto-subvinacea led to the establishment of populations in Carib-
bean Central America and in western Colombia; here they were isolated
1967 HAFFER: COLOMBIAN BIRDS 45
during the following periods of drought and were differentiated as Oenoe-
nas nigrirostris and Oenoenas goodsoni, respectively. A second invasion of
subvinacea made it sympatric with Oenoenas goodsoni in western Colombia
(Oenoenas s. berlepschi); in Central America it occupied the higher moun-
tain zones (Oenoenas s. subvinacea), thus being separated altitudinally from
T.f. florida
T. florida (subsp)
T.f. auricep
T. schrankii
Fic. 14. Distribution of the Tangara schrankii species group. Recently the
author has collected 7. johannae at the northern end of the Western Andes,
southeast of the Gulf of Uraba.
Plumage color key: Hatched, light emerald green; hatched and dotted, light
gold-green; sparsely dotted, yellow; densely dotted, blue; solid, black.
the lowland species Oenoenas nigrirostris. It is of interest to note that the
populations of both trans-Andean invasions deviate in the same manner
from the Amazonian parent form: Oe¢noenas goodsoni and O6enoenas sub-
vinacea berlepschi are smaller and lighter colored than the cis-Andean
representatives, the latter form showing these characters less pronounced,
because of the shorter period of isolation.
Tangara schrankit SPECIES GROUP
Figure 14
The trans-Andean representative of the Amazonian Tangara schranki
46 AMERICAN MUSEUM NOVITATES NO. 2294
is Tangara florida,1 which is restricted essentially to the area of the former
Caribbean Costa Rica Refuge and the Choco Refuge. Eisenmann (in /itt.)
informs me that a population morphologically intermediate between T.
f. florida and T. f auriceps, but nearer to the latter, occurs on the Ser-
rania del Darién in eastern Panama, west to Cerro Azul, not far east
of the Canal Zone. Hellmayr (1936) doubted that T°: schranku and T.
florida are even specifically distinct. Another trans-Andean bird of this
species group is Tangara johannae, the body coloration of which is very
close to that of 7: schranki. The pattern of the head color, however,
differs considerably from that of its relatives. It is assumed that T-
johannae represents an earlier invasion of the same proto-schranki stock
and today is sympatric with the younger arrival 7. florida auriceps in
part of its range.
TRIPLE INVASION
THE Trogon melanurus Species GRouP
Figure 15
In this group of closely related forms we count several trans-Andean
species but only one (7. melanurus) in the Amazonian region. It seems
possible that all trans-Andean forms originated from the same cis-Andean
stock by three consecutive invasions.
The oldest and most restricted trans-Andean forms are T. clathratus
and T. comptus of Caribbean Central America and western Colombia,
respectively. These forms appear to be specifically distinct from each
other and possibly represent the first trans-Andean invasion of proto-
melanurus. Although T. clathratus today is still restricted to Caribbean
Costa Rica and western Panama (Caribbean Costa Rica Refuge), T.
compius has subsequently extended its range from the Chocd Refuge to
include also the northern slope of the Western and Central Cordillera
of Colombia.
Trogon massena, which may represent the second invasion of proto-
melanurus stock, lives side by side with T. clathratus and T. comptus at the
present time. The Central American (7. m. massena) and west Colombian
(T. m. australis) populations are separated geographically by a gap in
the Atrato region. Both are morphologically very close and are best
considered still conspecific.
During a third, evidently rather recent, invasion, the cis-Andean popu-
lation occupied northern Colombia, and part of it was isolated in the
1Tangara schrankii anchicayae is a synonym of Tangara florida auriceps, as will be shown
by Lehmann in a forthcoming publication.
1967 HAFFER: COLOMBIAN BIRDS 47
Fic. 15. Distribution and speciation of the Trogon melanurus species group.
Several trans-Andean species originated from one Amazonian parent species
by three consecutive invasions: First: la, Trogon clathratus; 1b, T. comptus.
Second: 2a, T. massena massena: 2b, T. m. australis. Third: 3a, T. melanurus mac-
roura; 3b, T. m. mesurus; 3c, T. m. melanurus.
Plumage color key: Dotted, red; broadly hatched, green; wavy lines, vermiculated
black and white; narrowly hatched, wholly slaty or blackish (except 1a).
Nechi Refuge. It was here differentiated as 7. m. macroura, a form that
should be treated as conspecific with the cis-Andean 7. melanurus. Trogon
48 AMERICAN MUSEUM NOVITATES NO. 2294
TABLE 8
COMPARISON OF Cis-ANDEAN AND
Trans-ANDEAN Forest FAUNAS
Number of Species in Number of Trans-
Southeast Colombia Andean Species ”
(Amazonian Forest)
Tinamidae 9 5 (1+1+3)
Cracidae 10 7 (7+0+0)
Galbulidae 12 3 (1+1+1)
Bucconidae 14 10 (5+2+3)
Ramphastidae 8 4 (4+0+0)
Formicariidae 74 35 (17+5+ 13)
Pipridae 13 11 (44+2+5)
Cotingidae 23 13 (7+1+5)
“ The three columns in the parentheses indicate (1) those that are specifically distinct,
(2) those that are represented by a subspecifically distinct geographical isolate, and
(3) those species that range continuously from east to west.
massena macroura has extended its range into central Panama (where it is
sympatric with T. massena) and into western Colombia. In the latter area
the contact zone with 7. massena australis in the upper San Juan Valley
is not yet known.
Trogon melanurus has also crossed the Andes in the region of the Porculla
pass, northern Pert. The west-Ecuadorian form T. m. mesurus still ranges
today up into the subtropical zone (Chapman, 1926). It advanced north-
ward along the Pacific coast and met T. massena australis near the Colom-
bian boundary. Both forms may here be sympatric.
The above interpretation of the speciation within the Trogon melanurus
group (subgenus Curucujus) is in accord with the current taxonomic treat-
ment of the species involved and helps to solve certain problems as to
the status of the west and north Colombian forms. Zimmer (1948) pointed
out that the Chocd form australis might be specifically distinct from
T. massena and should possibly be considered conspecific with 7: m.
macroura. However, in my opinion, each of these forms is best considered
a member of two consecutive invasions of the same cis-Andean melanurus
stock.
BRIEF ANALYSIS OF THE CHOCO FAUNA
The center of the area occupied by the “Chocdé fauna” is the former
Chocé Refuge. Today it also includes the forested lowlands of north-
western Ecuador and eastern Panama. Western Panama should be in-
1967 HAFFER: COLOMBIAN BIRDS 49
cluded in the realm of the “Central American fauna,” although it goes
without saying that both faunas intermingle, and no fixed boundary
can be drawn in the central portion of Panama.
The fauna of northern Colombia and the humid middle Magdalena
Valley is also strongly influenced by the Chocdé fauna, but may be kept
apart and designated as the “Nechi fauna” (Cauca-Magdalena fauna
of Chapman, 1917) on account of several strongly differentiated species
confined to this region.
In the following quantitative survey of the Chocd fauna 332 species
have been considered (excluding all water and shore birds). One hun-
dred thirty-one species and subspecies (126+ 5, see semitabular summary
below), or 40 per cent of the total, are confined to the trans-Andean
region. Those forms that are only subspecifically differentiated (35) are
isolated by a gap from their cis-Andean relatives. Ninety forms are found
in both western Colombia and Central America; of these 31 have iso-
lated populations in the Choco region and in Central America, and 59
range continuously from western Colombia into Middle America. In the
latter group the majority show their derivation from the Chocdé Refuge
area by a rapidly decreasing abundance northward.
Twenty-two Central American forms have reached at least the north-
ern Choco area. Five of them have a geographical representative in
western Colombia and six in the Amazonian region.
A small group of the Nechi fauna (10) advanced into the northern
Chocé (lower Atrato Valley).
Another important element of the Chocé fauna is represented by those
species that have reached the Pacific lowlands by crossing the Andes in
northern Peri and southern Ecuador. Several of them are confined to
the southern part of the Pacific lowlands, others occupied the entire
Chocé region, and some even advanced into Central America.
Almost half of the Chocé fauna (43.1%) are “neutral” species. They
are continuously distributed from the Amazonian to the trans-Andean
lowlands, with no apparent major distributional break in northern
Colombia. Since gene flow is not interrupted, only clinal variation is
found in this group as one goes from Amazonia to western Colombia.
The composition of the Chocé fauna is in summary as follows:
Trans-Andean forms
Trans-Andean isolates (subspecies differentiation)............... 35 (10.6%)
Chocdéresiononly} 2.x 04+ os pod He 9 aye) Brace Pees 9
Chocé region plus Central America
Ranges discontinuous............. 60660 e ee eee eee 2
Ranges continuous... 0.0.0... 0.0 eee eee 24
Trans-Andean species (species differentiation). ..............-.-. 79 (23.8%)
50 AMERICAN MUSEUM NOVITATES NO. 2294
GHOGOFE PION OAD ac ee ee owe ene eo ow ge Se eee 20
Chocé region plus Central America
Ranges discontinuous. ........ 0.0.5.0 0c eee eee 25
Ranges continuous... ......... 0.06 cece ee eee 34
Trans-Andean genera (genus differentiation).............-....-4. 12 (3.6%)
Chocovresion only. 015% uses Shae ey et potas oS TAS 5
Chocé region plus Central America
Ranges discontinuous........... 5.00000 e ee eee 5
Ranges continuous:;) 6 gees bene erate aes ol 2
Central American elements advancing into northwestern
Colomiblast: osc aS eee ge oe Be ee aaa as Seat eed a! 22 (6.6%)
Without Chocéd representative .............. 00000-00088 11
With Choco representative... ...... 0.000000 cece eee M)
With cis-Andean representative. ..............0 00000005. 6
Nechi elements advancing into northern Chocé region........... 10 (3.0%)
Species reaching trans-Andean lowlands by crossing Andes
in northern Peri and southern Ecuador................... 31 (9.3%)
Advancing into southern Chocé region.................. 5
Like above but also coming around Andes in north and
found in northern Choco region. .............. 0.000004 10
Occupying whole Chocé area and in part advancing
into -Gentral America... 20st. 21a eee oes bee oe 16
“Neutral” species (cis- and trans-Andean populations in
contact with each other in northern Colombia today)........ 143 (43.1%)
Occupying the entire Chocd region.................4.5. 95
Only advancing into the northern Chocé................ 48
Total-number of species. <2 2..1 8 cg ae Es 332
The above survey differs sharply from Chapman’s interpretation
(1926, p. 58), especially by singling out those species and subspecies
that are actually restricted to the trans-Andean region and designating
as “neutral” those that are continuously distributed from east to west.
Moreover, a much smaller percentage of the fauna appears to be of
Central American origin. The large Chocéd Refuge, with access for the
Amazonian fauna from the north via the north Colombian lowlands and
from the south across the Andes, has contributed much more to the
Central American bird fauna than the other way around.
A comparison of the total numbers of cis-Andean and trans-Andean
species within a given family is of particular interest, since the per-
centage of Amazonian species that reached the Pacific lowlands throws
light on the problem of the efficiency of the Andes as a barrier to the
cis-Andean birds. A few figures have been assembled in table 8. From
these data it is obvious that at least half of the cis-Andean species, and
often far more, advanced into the trans-Andean region (exception, the
Galbulidae). Again, about 50 per cent of these were specifically differ-
entiated from their cis-Andean parent species. Apparently, then, at least
1967 HAFFER: COLOMBIAN BIRDS 51
half of the forest fauna of Colombian upper Amazonia was able to
reach the trans-Andean lowlands. The efficiency of the northern Andes
as a barrier to bird distribution was considerably reduced during the
humid climatic periods of the Pleistocene and post-Pleistocene.
SUMMARY
The main uplift of the Colombian Andes took place at the beginning
of the Pleistocene. At that time the present lowlands of southern Central
America and along the Pacific and Caribbean coasts of Colombia
emerged and were forest covered. The temperature gradient in at least
parts of the tropical latitudes during the glacial periods of the Pleisto-
cene was greater than it is today; for this reason the refrigeration af-
fected the higher latitudes and altitudes more (7°-8° C.) than the tropi-
cal lowlands (3°-4° C.). The latitudinal extent of the tropical lowlands
was not much less during the Pleistocene than it is today: the lowlands
of Colombia and great parts of Central America remained in the tropi-
cal zone (notwithstanding an extensive glaciation of the Central and
South American mountain ranges).
The faunas of the tropical lowlands were severely affected by sea-level
fluctuations and by alternating wet and dry periods during the Pleisto-
cene, caused by a contraction and expansion of the equatorial rain belt.
These climatic changes continued through post-Pleistocene time. During
the periods of drought the trans-Andean forest fauna was restricted to
rather small humid refuges: (a) on the Caribbean slope of Central
America (various refuges in Costa Rica, Nicaragua, Honduras); (b) on
the Pacific slope of southwestern Costa Rica and adjacent Panama
(“Chiriqui Refuge”); (c) along the Pacific coast of Colombia (“Chocé
Refuge”); and (d) at the foot of the northern slope of the Western and
Central Andes of Colombia (“Nechi Refuge’). Strongly marked endemic
forms originated in these refuges during periods of geographic isolation
resulting from drought, at which time the connection of the trans- and
cis-Andean forests was interrupted in the north Colombian lowlands.
It is concluded that the uplift of the Colombian Andes was only in-
directly responsible for the development of the numerous Central Ameri-
can and west Colombian endemic species. The direct causation for their
development was the repeated change of dry and humid periods during
the Pleistocene and post-Pleistocene. These climatic changes permitted
and interrupted repeatedly the contact of the trans- and cis-Andean
populations in the north Colombian lowlands through the expansion
and shrinkage of the forests. In this way an increasing number of small
founder populations was able to reach the trans-Andean forests. The
52 AMERICAN MUSEUM NOVITATES NO. 2294
high concentration of endemic species in the tropical lowland forests of
western Colombia and Central America is explained by a gradual ac-
cumulation of isolates in the trans-Andean forest refuges.
Numerous Chocé elements extended their ranges to Central America,
in some cases forming another isolate in the refuges along the Caribbean
slope. On the other hand, only a few Central American species advanced
into northern Colombia.
Zones of allopatric hybridization are developed at the eastern margin
of the Caribbean Costa Rica Refuge in western Panama and at the
northern margin of the Chocéd Refuge in the Uraba region of north-
western Colombia. These zones are probably of very recent origin. ‘The
hybridization of Pteroglossus t. torquatus X P. (torquatus) sanguineus and of
Galbula r. ruficauda X G. (ruficauda) melanogenia is described in detail.
Double invasions were responsible for the present co-existence of
Columbia (Oenoenas) goodsoni and Columbia (O.) subvinacea berlepschi and
of Tangara johannae and T. florida in western Colombia. A triple invasion
caused the speciation within the black-tailed Trogon melanurus group.
The majority of the Amazonian forest birds that reached the trans-
Andean lowlands came around the Andes from the north. However, a
small group seems to have followed the upper Marajion Valley to cross
the Andes in northern Pert or southern Ecuador (or both) during wet
climatic periods of the past.
A quantitative analysis of the Chocé fauna is included. A comparison
of the number of trans- and cis-Andean species of certain families of
forest birds shows that at least half of the upper Amazonian fauna
reached the trans-Andean forests.
LITERATURE CITED
Bancs, OuTRAM, AND THOMAS BARBOUR
1922. Birds from Darien. Bull. Mus. Comp. Zool., vol. 65, pp. 191-229.
BELDINnG, HERBERT F.
1955. Geological development of the Colombian Andes. Proc. Conf. Latin-
Amer. Geol., Univ. Texas, pp. 43-63.
BIGELow, R. S.
1965. Hybrid zones and reproductive isolation. Evolution, vol. 19, pp.
449-458.
BorrERO, José I., anp JoRGE HERNANDEZ
1957. Informe preliminar sobre aves y mamiferos de Santander, Colombia.
An. Soc. Biol., vol. 7, pp. 197-202.
Borrero, José I., ANTONIO OLIVARES, AND JORGE HERNANDEZ
1962. Notas sobre aves de Colombia. Caldasia, vol. 8, pp. 585-601.
Bimrct, Hans
1961. Historia geolégica de Colombia. Rev. Acad. ol. Cien. Ex., Fis. y
Nat., vol. 11, pp. 137-191.
1967 HAFFER: COLOMBIAN BIRDS 53
CARRIKER, MELBouRNE A., JR.
1910. An annotated list of the birds of Costa Rica including Cocos Island.
Ann. Carnegie Mus., vol. 6, pp. 314-915.
Cassin, JOHN
1860. Catalogue of birds collected during a survey of a route for a ship
canal across the Isthmus of Darien, by order of the Government of the
United States, made by Lieut. N. Michler, of the U. S. Topographi-
cal Engineers, with notes and descriptions of new species. Proc. Acad.
Nat. Sci. Philadelphia, vol. 12, pp. 132-144.
CHAPMAN, FRANK M.
1917. The distribution of bird-life in Colombia: a contribution to a bio-
logical survey of South America. Bull. Amer. Mus. Nat. Hist., vol.
36, pp. 1-729.
1923. The distribution of the motmots of the genus Momotus. Ibid., vol. 48,
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